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The mushroom body output encodes behavioral decision during sensory-motor transformation

2023; Elsevier BV; Volume: 33; Issue: 19 Linguagem: Inglês

10.1016/j.cub.2023.08.016

1879-0445

Cansu Arican, Felix Johannes Schmitt, Wolfgang Rößler, Martin F. Strube‐Bloss, Martin Paul Nawrot,

Plant Molecular Biology Research

Animals form a behavioral decision by evaluating sensory evidence on the background of past experiences and the momentary motivational state. In insects, we still lack understanding of how and at which stage of the recurrent sensory-motor pathway behavioral decisions are formed. The mushroom body (MB), a central brain structure in insects1Strausfeld N.J. Sinakevitch I. Brown S.M. Farris S.M. Ground plan of the insect mushroom body: functional and evolutionary implications.J. Comp. Neurol. 2009; 513: 265-291https://doi.org/10.1002/cne.21948Crossref PubMed Scopus (168) Google Scholar and crustaceans,2Strausfeld N.J. Wolff G.H. Sayre M.E. Mushroom body evolution demonstrates homology and divergence across Pancrustacea.eLife. 2020; 9: 1-46https://doi.org/10.7554/eLife.52411Crossref Scopus (25) Google Scholar,3Harzsch S. Krieger J. 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Essential role of the mushroom body in context-dependent CO2 avoidance in Drosophila.Curr. Biol. 2013; 23: 1228-1234https://doi.org/10.1016/j.cub.2013.05.029Abstract Full Text Full Text PDF PubMed Scopus (68) Google Scholar Here, we co-analyzed a defined feeding behavior and simultaneous extracellular single-unit recordings from MB output neurons (MBONs) in the cockroach in response to timed sensory stimulation with odors. We show that clear neuronal responses occurred almost exclusively during behaviorally responded trials. Early MBON responses to the sensory stimulus preceded the feeding behavior and predicted its occurrence or non-occurrence from the single-trial population activity. Our results therefore suggest that at its output, the MB does not merely encode sensory stimulus valence. We hypothesize instead that the MB output represents an integrated signal of internal state, momentary environmental conditions, and experience-dependent memory to encode a behavioral decision.